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Effect of oocyte-secreted factors on porcine in vitro maturation, cumulus expansion and developmental competence of parthenotes

Published online by Cambridge University Press:  27 July 2011

Ma. Ninia L. Gomez
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul, Korea.
Jung Taek Kang
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul, Korea.
Ok Jae Koo
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul, Korea.
Su Jin Kim
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul, Korea.
Dae Kee Kwon
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul, Korea.
Sol Ji Park
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul, Korea.
Mohammad Atikuzzaman
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul, Korea.
So Gun Hong
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul, Korea.
Goo Jang
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul, Korea.
Byeong Chun Lee*
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine, Seoul National University, Seoul 151–742, Korea.
*
All correspondence to: Byeong Chun Lee. Department of Theriogenology and Biotechnology, College of Veterinary Medicine, Seoul National University, Seoul 151–742, Korea. Tel: +822 880 1269. Fax: +822 873 1269. E-mail: bclee@snu.ac.kr

Summary

The oocyte is known from recent studies in the mouse, cow, sheep and human to be a central regulator of follicular cell function. However, in the pig, little information is known about the regulation of cumulus expansion by oocyte-secreted factors and oocyte quality. We investigated the possible effects of oocyte-secreted factors during in vitro maturation on cumulus expansion and on porcine oocytes as judged by subsequent embryonic development after parthenogenetic activation. Cumulus–oocyte complexes (COC) from antral follicles of pig ovaries collected from a local abattoir were divided into control and treatment groups and were cultured in tissue culture medium 199 supplemented with follicle-stimulating hormone. Treatment groups consisted of increasing numbers of denuded oocytes (DO) co-cultured with COC (at ratios of COC to DO of 1:1, 1:2, 1:3, 1:4 and 1:5). After incubation for 44 h, cumulus expansion and maturation rates were assessed and oocytes were activated parthenogenetically. Cumulus expansion in the 1 COC:4 DO and 1 COC:5 DO groups was low and altered because full dispersion of the outer layer did not occur. Cell viability was not affected, as measured by the automated cell counter, but scanning electron microscopy revealed only a scanty extracellular matrix. Blastocyst rate was significantly higher in the 1 COC:4 DO (34.4%) and in the 1 COC:5 DO (34.9%) groups (p < 0.05) when compared with other groups. Maturation rate, cleavage rate and total cell number showed no significant difference between control and treatment groups. Amplification by reverse transcription polymerase chain reaction (RT-PCR) showed up-regulation of growth differentiation factor 9 (GDF9) in the cumulus cells in the 1 COC:4 DO group at 44 h. We conclude that denuded porcine oocytes could improve the maturation of COC as evidenced by increased blastocyst development in the 1 COC:4 DO, even though cumulus expansion was poor. This improvement could be a result of the GDF9 up-regulation.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

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References

Aaltonen, J., Laitinen, M.P., Vuojolainen, K., Jaatinen, R., Horelli-Kuitunen, N., Seppa, M.P., Louhio, L., Tuuri, T., Sjoberg, J., Butzow, R., Hovata, O., Dale, L. & Ritvos, O. (1999). Human growth differentiation factor 9 (GDF9) and its novel homolog GDF9B are expressed in oocytes during early folliculogenesis. J. Clin. Endocrinol. Metab. 84, 2744–50.Google ScholarPubMed
Chang, H., Brown, C.W. & Matzuk, M.M. (2002). Genetic analysis of the mammalian transforming growth factor-beta superfamily. Endocr. Rev. 23, 787823.CrossRefGoogle ScholarPubMed
Cooper, D.K.C., Ye, Y., Rolf, L.J. & Zudhi, N. (1991). The pig as potential organ donor for man. In Xenotransplantation, 1st edn (eds. Cooper, D.K.C., Kemp, E., Reemtsma, K. & White, D.J.G.), pp. 481500. Heidelberg: Springer.CrossRefGoogle Scholar
Cooper, D.K., Gollackner, B. & Sachs, D.H. (2002). Will the pig solve the transplantation backlog? Annu. Rev. Med. 53, 133–47.CrossRefGoogle ScholarPubMed
Davis, G.H., McEwan, J.C., Fennessy, P.F., Dodds, K.G., McNatty, K.P. & , O W.S. (1992). Infertility due to bilateral ovarian hypoplasia in sheep homozygous (FecXI FecXI) for the Inverdale prolificacy gene located on the X chromosome. Biol. Reprod. 46, 636–40.CrossRefGoogle ScholarPubMed
Di Pasquale, E., Beck-Peccoz, P. & Persani, L. (2004). Hypergonadotropic ovarian failure associated with an inherited mutation of human bone morphogenetic protein-15 (BMP15) gene. Am. J. Hum. Genet. 75, 106–11.CrossRefGoogle ScholarPubMed
Diaz, F.J., Wigglesworth, K. & Eppig, J.J. (2007). Oocytes determine cumulus cell lineage in mouse ovarian follicles. J. Cell. Sci. 120, 1330–40.CrossRefGoogle ScholarPubMed
Dixit, H., Rao, L.K., Padmalatha, V.V., Kanakavalli, M., Deenadayal, M., Gupta, N., Chakrabarty, B. & Singh, L. (2006). Missense mutations in the BMP15 gene are associated with ovarian failure. Hum. Genet. 119, 408–15.CrossRefGoogle ScholarPubMed
Dong, J., Albertini, D.F., Nishimori, K., Kumar, T.R., Lu, N. & Matzuk, M.M. (1996). Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383, 531–5.CrossRefGoogle ScholarPubMed
Dragovic, R.A., Ritter, L.J., Schulz, S.J., Amato, F., Thompson, J.G., Armstrong, D.T. & Gilchrist, R.B. (2007). Oocyte-secreted factor activation of SMAD 2/3 signaling enables initiation of mouse cumulus cell expansion. Biol. Reprod. 76, 848–57.CrossRefGoogle ScholarPubMed
Dube, J.L., Wang, P., Elvin, J., Lyons, K.M., Celeste, A.J. & Matzuk, M.M. (1998). The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes. Mol. Endocrinol. 12, 1809–17.CrossRefGoogle ScholarPubMed
Elvin, J.A., Yan, C., Wang, P., Nishimori, K. & Matzuk, M.M. (1999). Molecular characterization of the follicle defects in the growth differentiation factor 9-deficient ovary. Mol. Endocrinol. 13, 1018–34.CrossRefGoogle ScholarPubMed
Eppig, J.J. (2001). Oocyte control of ovarian follicular development and function in mammals. Reproduction 122, 829–38.CrossRefGoogle ScholarPubMed
Fitzpatrick, S.L., Sindoni, D.M., Shughrue, P.J., Lane, M.V., Merchenthaler, I.J. & Frail, D.E. (1998). Expression of growth differentiation factor-9 messenger ribonucleic acid in ovarian and nonovarian rodent and human tissues. Endocrinology 139, 2571–8.CrossRefGoogle ScholarPubMed
Galloway, S.M., McNatty, K.P., Cambridge, L.M., Laitinen, M.P.E., Juengel, J.L., Jokiranta, T.S., McLaren, R.J., Luiro, K., Dodds, K.G., Montgomery, G.W., Beattie, A.E., Davis, G.H. & Ritvos, O. (2000). Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat. Genet. 25, 279–83.CrossRefGoogle Scholar
Gilchrist, R.B. & Thompson, J.G. (2007). Oocyte maturation: emerging concepts and technologies to improve developmental potential in vitro. Theriogenology 67, 615.CrossRefGoogle ScholarPubMed
Gilchrist, R.B., Ritter, L.J. & Armstrong, D.T. (2004). Oocyte–somatic cell interactions during follicle development in mammals. Anim. Reprod. Sci. 82–83, 431–46.CrossRefGoogle ScholarPubMed
Gilchrist, R.B., Ritter, L.J., Myllymaa, S., Kaivo-Oja, N., Dragovic, R.A., Hickey, T.E., Ritvos, O. & Mottershead, D.G. (2006). Molecular basis of oocyte-paracrine signaling that promotes granulosa cell proliferation. J. Cell. Sci. 119, 3811–21.CrossRefGoogle ScholarPubMed
Gilchrist, R.B., Lane, M. & Thompson, J.G. (2008). Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum. Reprod. 14, 159–77.Google ScholarPubMed
Hanrahan, J.P., Gregan, S.M., Mulsant, P., Mullen, M., Davis, G.H., Powell, R. & Galloway, S.M. (2004). Mutations in the genes for oocyte-derived growth factors GDF9 and BMP15 are associated with both increased ovulation rate and sterility in Cambridge and Belclare sheep (Ovis aries). Biol. Reprod. 70, 900–9.CrossRefGoogle ScholarPubMed
Hsieh, C.H., Tang, P.C., Chang, W.H., Weng, Y.C., Sha, S.W., Tseng, J.K., Chang, L.H. & Ju, J.C. (2006). The kinase inhibitor indirubin-3¢-oxime prevents germinal vesicle breakdown and reduces parthenogenetic development of pig oocytes. Theriogenology 65, 744–56.CrossRefGoogle ScholarPubMed
Hussein, T.S., Froiland, D.A., Amato, F., Thompson, J.G. & Gilchrist, R.B. (2005). Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. J. Cell. Sci. 118, 5257–68.CrossRefGoogle ScholarPubMed
Hussein, T.S., Thompson, J.G. & Gilchrist, R.B. (2006). Oocyte-secreted factors enhance oocyte developmental competence. Dev. Biol. 296, 514–21.CrossRefGoogle ScholarPubMed
Juengel, J.L., Hudson, N.L., Heath, D.A., Smith, P., Reader, K.L., Lawrence, S.B., O'Connell, A.R., Laitinen, M.P.E., Cranfield, M., Groome, N.P., Ritvos, O. & McNatty, K.P. (2002). Growth differentiation factor 9 and bone morphogenetic protein 15 are essential for ovarian follicular development in sheep. Biol. Reprod. 67, 1777–89.CrossRefGoogle ScholarPubMed
Juengel, J.L., Hudson, N.L., Whiting, L. & McNatty, K.P. (2004). Effects of immunization against bone morphogenetic protein 15 and growth differentiation factor 9 on ovulation rate, fertilization, and pregnancy in ewes. Biol. Reprod. 70, 557–61.CrossRefGoogle ScholarPubMed
Juengel, J.L. & McNatty, K.P. (2005). The role of proteins of the transforming growth factor-beta superfamily in the intraovarian regulation of follicular development. Hum. Reprod. Update 11, 143–60.CrossRefGoogle ScholarPubMed
Kuijk, E., du Puy, L., van Tol, H., Haagsman, H., Colenbrander, B. & Roelen, B. (2007). Validation of reference genes for quantitative RT-PCR studies in porcine oocytes and preimplantation embryos. BMC Dev. Biol. 7, 58.CrossRefGoogle ScholarPubMed
Kure-bayashi, S., Miyake, M., Okada, K. & Kato, S. (2000). Successful implantation of in vitro matured, electro-activated oocytes in the pig. Theriogenology 53, 1105–19.CrossRefGoogle ScholarPubMed
Laissue, P., Christin-Maitre, S., Touraine, P., Kuttenn, F., Ritvos, O., Aittomaki, K., Bourcigaux, N., Jacquesson, L., Bouchard, P., Frydman, R., Dewailly, D., Reyss, A.C., Jeffery, L., Bachelot, A., Massin, N., Fellous, M. & Veitia, R.A. (2006). Mutations and sequence variants in GDF9 and BMP15 in patients with premature ovarian failure. Eur. J. Endocrinol. 154, 739–44.CrossRefGoogle ScholarPubMed
Latham, K.E., Doherty, A.S., Scott, C.D. & Schultz, R.M. (1994). Igf2r and Igf2 gene expression in androgenetic, gynogenetic, and parthenogenetic preimplantation mouse embryos: absence of regulation by genomic imprinting. Genes Dev. 8, 290–9.CrossRefGoogle ScholarPubMed
McGrath, S.A., Esquela, A.F. & Lee, S.J. (1995). Oocyte-specific expression of growth/differentiation factor-9. Mol. Endocrinol. 9, 131–6.Google ScholarPubMed
McNatty, K.P., Moore, L.G., Hudson, N.L., Quirke, L.D., Lawrence, S.B., Reader, K., Hanrahan, J.P., Smith, P., Groome, N.P., Laitinen, M., Ritvos, O. & Juengel, J.L. (2004). The oocyte and its role in regulating ovulation rate: a new paradigm in reproductive biology. Reproduction 128, 379–86.CrossRefGoogle Scholar
McNatty, K.P., Hudson, N.L., Whiting, L., Reader, K.L., Lun, S., Western, A., Heath, D.A., Smith, P., Moore, L.G. & Juengel, J.L. (2007). The effects of immunizing sheep with different BMP15 or GDF9 peptide sequences on ovarian follicular activity and ovulation rate. Biol. Reprod. 76, 552–60.CrossRefGoogle ScholarPubMed
Montgomery, G.W., Zhao, Z.Z., Marsh, A.J., Mayne, R., Treloar, S.A., James, M., Martin, N.G., Boomsma, D.I. & Duffy, D.L. (2004). A deletion mutation in GDF9 in sisters with spontaneous DZ twins. Twin Res. Hum. Genet. 7, 548–55.CrossRefGoogle ScholarPubMed
Mulsant, P., Lecerf, F., Fabre, S., Schibler, L., Monget, P., Lanneluc, I., Pisselet, C., Riquet, J., Monniaux, D., Callebaut, I., Cribiu, E., Thimonier, J., Teyssier, J., Bodin, L., Cognie, Y., Chitour, N. & Elsen, J.M. (2001). Mutation in bone morphogenetic protein receptor-IB is associated with increased ovulation rate in Booroola Merino ewes. Proc. Natl. Acad. Sci. USA 98, 5104–9.CrossRefGoogle ScholarPubMed
Otsuka, F., Yao, Z., Lee, T.H., Yamamoto, S., Erickson, G.F. & Shimasaki, S. (2000). Bone morphogenetic protein-15: identification of target cells and biological functions. J. Biol. Chem. 275, 39523–8.CrossRefGoogle ScholarPubMed
Palmer, J.S., Zhao, Z.Z., Hoekstra, C., Hayward, N.K., Webb, P.M., Whiteman, D.C., Martin, N.G., Boomsma, D.I., Duffy, D.L. & Montgomery, G.W. (2006). Novel variants in growth differentiation factor 9 in mothers of dizygotic twins. J. Clin. Endocrinol. Metab. 91, 4713–6.CrossRefGoogle ScholarPubMed
Prather, R.S., Hawley, R.J., Carter, D.B., Lai, L. & Greenstein, J.L. (2003). Transgenic swine for biomedicine and agriculture. Theriogenology 59, 115–23.CrossRefGoogle ScholarPubMed
Prochazka, R., Nagyova, E., Rimkevicova, Z., Nagai, T., Kikuchi, K. & Motlik, J. (1991). Lack of effect of oocytectomy on expansion of the porcine cumulus. J. Reprod. Fertil. 93, 569–76.CrossRefGoogle ScholarPubMed
Salustri, A., Ulisse, S., Yanagishita, M. & Hascall, V.C. (1990a). Hyaluronic acid synthesis by mural granulosa cells and cumulus cells in vitro is selectively stimulated by a factor produced by oocytes and by transforming growth factor-beta. J. Biol. Chem. 265, 19517–23.CrossRefGoogle ScholarPubMed
Salustri, A., Yanagishita, M. & Hascall, V.C. (1990b). Mouse oocytes regulate hyaluronic acid synthesis and mucification by FSH-stimulated cumulus cells. Dev. Biol. 138, 2632.CrossRefGoogle ScholarPubMed
Shimasaki, S., Moore, R.K., Otsuka, F. & Erickson, G.F. (2004). The bone morphogenetic protein system in mammalian reproduction. Endocr. Rev. 25, 72101.CrossRefGoogle ScholarPubMed
Souza, C.J., MacDougall, C., Campbell, B.K., McNeilly, A.S. & Baird, D.T. (2001). The Booroola (FecB) phenotype is associated with a mutation in the bone morphogenetic receptor type 1 B (BMPR1B) gene. J. Endocrinol. 169, R16.CrossRefGoogle ScholarPubMed
Su, Y.Q., Wu, X., O'Brien, M.J., Pendola, F.L., Denegre, J.N., Matzuk, M.M. & Eppig, J.J. (2004). Synergistic roles of BMP15 and GDF9 in the development and function of the oocyte–cumulus cell complex in mice: genetic evidence for an oocyte–granulosa cell regulatory loop. Dev. Biol. 276, 6473.CrossRefGoogle ScholarPubMed
Su, Y.Q., Sugiura, K., Wigglesworth, K., O'Brien, M.J., Affourtit, J.P., Pangas, S.A., Matzuk, M.M. & Eppig, J.J. (2008). Oocyte regulation of metabolic cooperativity between mouse cumulus cells and oocytes: BMP15 and GDF9 control cholesterol biosynthesis in cumulus cells. Development 135, 111–21.CrossRefGoogle ScholarPubMed
Vanderhyden, B.C. (1993). Species differences in the regulation of cumulus expansion by an oocyte-secreted factor(s). J. Reprod. Fertil. 98, 219–27.CrossRefGoogle ScholarPubMed
Vanderhyden, B.C., Caron, P.J., Buccione, R. & Eppig, J.J. (1990). Developmental pattern of the secretion of cumulus expansion-enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation. Dev. Biol. 140, 307–17.CrossRefGoogle ScholarPubMed
Vanderhyden, B.C., Cohen, J.N. & Morley, P. (1993). Mouse oocytes regulate granulosa cell steroidogenesis. Endocrinology 133, 423–6.CrossRefGoogle ScholarPubMed
Wilson, T., Wu, X.Y., Juengel, J.L., Ross, I.K., Lumsden, J.M., Lord, E.A., Dodds, K.G., Walling, G.A., McEwan, J.C., O'Connell, A.R., McNatty, K.P. & Montgomery, G.W. (2001). Highly prolific Booroola sheep have a mutation in the intracellular kinase domain of bone morphogenetic protein IB receptor (ALK-6) that is expressed in both oocytes and granulosa cells. Biol. Reprod. 64, 1225–35.CrossRefGoogle ScholarPubMed
Yan, C., Wang, P., DeMayo, J., DeMayo, F.J., Elvin, J.A., Carino, C., Prasad, S.V., Skinner, S.S., Dunbar, B.S., Dube, J.L., Celeste, A.J. & Matzuk, M.M. (2001). Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol. Endocrinol. 15, 854–66.CrossRefGoogle ScholarPubMed
Yeo, C.X., Gilchrist, R.B., Thompson, J.G. & Lane, M. (2008). Exogenous growth differentiation factor 9 in oocyte maturation media enhances subsequent embryo development and fetal viability in mice. Hum. Reprod. 23, 6773.CrossRefGoogle ScholarPubMed
Yeo, C.X., Gilchrist, R.B. & Lane, M. (2009). Disruption of bidirectional oocyte-cumulus paracrine signalling during in vitro maturation reduces subsequent mouse oocyte developmental competence. Biol. Reprod. 80, 1072–80.CrossRefGoogle ScholarPubMed
Yi, S.E., LaPolt, P.S., Yoon, B.S., Chen, J.Y., Lu, J.K. & Lyons, K.M. (2001). The type I BMP receptor BmprIB is essential for female reproductive function. Proc. Natl. Acad. Sci. USA 98, 7994–9.CrossRefGoogle ScholarPubMed
Zhu, G., Guo, B., Pan, D., Mu, Y. & Feng, S. (2008). Expression of bone morphogenetic proteins and receptors in porcine cumulus-oocyte complexes during in vitro maturation. Anim. Reprod. Sci. 104, 275–83.CrossRefGoogle ScholarPubMed